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[REE CEDAR RUST FUNGI, THEIR LIFE 
HISTORIES AND THE DISEASES 
WHICH THEY PRODUCE 



A THESIS 

Presented to the Faculty of the Graduate School 
op Cornell University for the Degree of 

DOCTOR OF PHILOSOPHY 



BY 

JAMES LeROY WEIMER 



Reprint from Cornell University Agricultural Experiment Station Bulletin 390, 

May, 19 1 7 



THREE CEDAR RUST FUNGI, THEIR LIFE 

HISTORIES AND THE DISEASES 

WHICH THEY PRODUCE 



A THESIS 

Presented to the Faculty of the Graduate School 

of Cornell University for the Degree of 

DOCTOR OF PHILOSOPHY 



BY 

JAMES LeROY WEIMER 



Reprint from Cornell University Agricultural Experiment Station Bulletin 390, 

May, 19 1 7 






In exchange 



CONTENTS 

PAGE 

Hosts 509 

The disease caused by Gymnosporangium Juniperi-virginianae 510 

History and geographical distribution 510 

Economic importance 510 

Nature of losses 511 

Symptoms 513 

On cedar 513 

On apple 514 

On the leaves 514 

( )n the fruit 515 

On the twigs 515 

Etiology 515 

Nomenclature 515 

Life history 515 

Telial stage 515 

Inoculation of cedar 515 

Susceptibility of individual trees 517 

Infection period 517 

Mycelium and haustoria 518 

Development of telial horns 518 

Teliospore germination 520 

Dissemination of basidiospores 523 

Germination of basidiospores 524 

Aecial stage 524 

Inoculation and infection of apple 524 

Effect of environmental factors 525 

Strains of the fungus 526 

Varietal susceptibility of apple 526 

Pycnia ... 527 

Aecia 528 

Germination of aeciospores ■ 529 

The disease caused by Gymnosporangium globosum 531 

Symptoms 531 

On cedar 531 

On quince 532 

On pear 532 

On Crataegus 534 

Etiology 535 

Nomenclature 535 

Life history 535 

Telial stage 536 

Development of telial horns 536 

Aecial stage 537 

Aeciospore germination 537 

Inoculation of cedar trees 537 

The disease caused by Gymnosporangium clavipes 539 

Symptoms 539 

On cedar 539 

On quince 539 

On Crataegus 541 

Etiology 543 

Nomenclature 543 

Life history 543 

Telial stage 543 

Development of telial sori 543 

Teliospore germination 545 

Aecial stage 546 

Literature cited 548 

5<>7 



THREE CEDAR RUST FUNGI 

THEIR LIFE HISTORIES AND THE DISEASES THEY PRODUCE « 

James LeRoy Weimer 

The three fungi considered in these investigations are Gymnosporangium 
Juniperi-virginianae Schw., Gymnosporangium globosum Farlow, and 
Gymnosporangium clavipes C. & P. Except for a discussion of the hosts 
concerned, the fungi, together with the diseases that they produce, are 
treated separately. 

HOSTS 

Certain species of the genus Juniperus on the one hand and various 
species of the family Rosaceae on the other, serve as hosts for the alternate 
stages in the life cycles of the fungi named above. In the telial stage all 
three species occur on Juniperus virginiana L. Kern (iqii) 2 reports 
G. Juniperi-virginianae and G. globosum also on /. barbadensis L., and 
G. clavipes on ./. communis L. Several horticultural varieties of /. vir- 
giniana are also known to be hosts. In this discussion, however, only 
/. virginiana will be considered as the telial host since it is the only species 
common in central New York State, in which locality the investigations 
were made. 

In their aecial stage these fungi occur on certain closely related members 
of the family Rosaceae. Among these are the cultivated and the wild 
varieties of apple (Pyrus malus L.) and crab apple (Pyrus coronaria L.), 
quince (Cydonia vulgaris Pers.), pear (Pyrus communis L.), June berry 
(Amelanchier spp.), mountain ash (Sorbus spp.), and numerous species of 
Crataegus. 3 



1 Also presented to the Faculty of the Graduate School of Cornell University. May, 1916, as a major 
thesis in partial fulfillment of the requirements for the degree of doctor of philosophy. 

Author's acknowledgments. Grateful acknowledgment for assistance and suggestions is made to 
Professor H. H. Whetzel; to Dr. V. B. Stewart for help and criticism in preparation of the manuscript; 
and especially to Dr. Donald Reddick, under whose immediate direction the work was performed. 

2 Dates in parenthesis refer to Literatnre cited, page 548. 

3 For a more complete list of hosts see Kern (1911). 



509 



5io Bulletin - 390 



THE DISEASE CAUSED BY GYMNOSPORANGIUM JUNIPERI- 
VIRGINIANAE 

The disease caused by the fungus Gymnosporangium J uniperi-vir- 
ginianae is generally known as cedar rust, although the galls are referred 
to as cedar apples or, more rarely, as cedar flowers. The term apple rust 
is most commonly applied to the aecial stage. Other names, such as 
leaf rust, stem rust, fruit rust, and orchard rust, are sometimes used to 
designate this disease. 

HISTORY AND GEOGRAPHICAL DISTRIBUTION 

The fungus is native to North America and has never been reported 
elsewhere so far as the writer has knowledge. Although it had already 
been known for a long time, it received but little attention prior to the 
work of Farlow in 1880. During the last decade, numerous investigations 
have been conducted bearing on the life history of the organism and on 
methods of control of the disease on the apple. 

The apple rust stage is widely distributed throughout the eastern 
half of the United States wherever cedar and apple occur together. 4 

ECONOMIC IMPORTANCE 

Owing to the fact that cedar trees occur in considerable numbers in but 
few States, apple rust has become of great economic importance only in 
certain localities. In some of the Southern States, where cedars grow in 
close proximity to the orchards, the disease causes an annual loss aggre- 
gating several thousand dollars, and there is considerable evidence that it 
is becoming more destructive each year. Pammel (1905) had never 
observed this rust on cultivated apples in Iowa prior to 1905. Emerson 
(1905), speaking of conditions in Nebraska, G. E. Stone (191 1) in Massa- 
chusetts, and Giddings and Neal (191 2) in West Virginia, state that the 
disease is becoming more serious each year. Stewart (19 10) records several 
outbreaks in New York State, but says that the disease is rarely of much 
economic importance. R. E. Stone (1908) in Alabama, and Reed and 
Crabill (191 5) in Virginia, list this as the most serious disease of apples in 
their respective States. In central New York the disease is very common 
on wild species of apple but is seldom found on cultivated varieties. The 
writer had two orchards under observation during the seasons of 1914 
and 191 5, one of which contained numerous cedar trees that were affected 
with G. Juniperi-virginianac, G. globosum, and 67. clavipes, while the other 
was only about a half mile distant from a cedar grove that was severely 

'For limits of geographical distribution see Kern (ion). 



Three Cedar Rust Fungi 



Si i 



infested with these three species of rust fungi. No affected apple leaves 
or fruit were found in either orchard. A few affected leaves and two 
affected apples were found in the Cornell University orchard in 1914. 




Fig 136 G\LLS OF gymnosporangium juniperi-virginianae 

The galls are m the winter condition and show the depressions from which the tehal horns 
ine gaiis are protrude in the following spring 

NATURE OF LOSSES 

Although the greatest loss from this rust occurs on the apple, cedar 
trees also mav be materially injured. The injury to apple trees caused 
by the disease is largely due to premature defoliation and to a reduction 



5i2 



111 I 1 ETI] 



in the vital activities of the less seriously affected leaves. Premature 
defoliation year after year greatly reduces the vigor of the trees and 
death may finally result. -Reed, Gooley, and Crabill (1914) state that 




Fig. 



137. TKUAI. HORNS OF GYMNOSPORANGIUM JUNIPERI-VIRGINIANAE 

The tclial horjis are shown as they appear after one gelatinization period 



where the disease is severe for several years in succession the trees make 
but little growth, become much weakened, and are more subject to attacks 
of insects and of other fungi. Another source of loss is due to the deforma- 
tion of the affected fruit, such fruit in most cases being unsatisfactory for 



Three Cedar Ru&t Fungi 



513 



market. The young twigs may also become affected 5 and die; in many 
such cases death of a tree may ensue before it reaches bearing age. 



SYMPTOMS 

On cedar 
On the cedar tree the first evidence of the disease caused by G. Jiuripcri- 
virginianae is a minute 
greenish swelling on the 
leaf, usually noticeable 
first on its upper, or 
inner, surface. The af- 
fected part of the leaf 
enlarges rapidly and be- 
comes gradually darker 
in color, and by the last 
of September a nearly 
full-grown cedar apple 
is f( irmed. At this time 
the gall is greenish 
brown in color, from 
globose to reniform in 
shape, and of a diam- 
eter varying from two 
millimeters to five cen- 
timeters. In New Y< >rk 
State the slight pit-like 
depressions in the outer 
surface of the gall ap- 
pear about October 1 
(fig. 136). In the fol- 
lowing spring the telial 
horns protrude in mi 
the depressions. These 
horns are golden brown 
in color and cylindric- 
acuminate in shape ( fig. 
137). During warm 
spring rains they gelatinize and enlarge about two to three times (fig. 138). 
Later the galls die, but often they remain attached to the cedar tree for 
a year or more. 

5 Twig infections of a wild variety of apple were verv common at Ithaca, New York, during the summer 
of 1914. 




Fig. 13S. gali. of 



Tlu' telial horn; 



GYMNOSPORANGIUM JUNIPERI-VIR- 
GINIANAE 

are shown as fully gelatinized 



514 



Bulletin 390 



On apple 
On the leaves 

The first evidence of infection by G. J uniperi-virginianae on the apple leaf 
is the appearance of very small greenish yellow spots about one-half 
millimeter in diameter. These spots gradually enlarge and the color 
changes to orange-yellow often bordered by concentric red bands (fig. 139') . 




FlG. 139. APPLE LEAVES AFFECTED WITH GYMNOSPORANGIUM JUNIPERI- 

VIRGINIANAE 

The characteristic lesions of the rust are shown on both sides of the leaves 

In these lesions minute yellow pyenia soon appear, which vary in number 
according to the size of the affected area. After a few days the pyenia 
exude droplets of a yellow, sweetish substance, and soon afterward they 
turn black. The underside of the lesion becomes hypertrophied about this 
time and the aecia soon appear. These may be arranged in a circle near 
the margin of the swollen area or they may be scattered over the lesion. 



Three Cedar Rust Fungi 



5*5 



On the fruit 

The lesions on the fruit are similar to those on the leaves except that 
normally they are larger and bear a larger number of aecia (fig. 140). 
The spots are yellow and wrinkled, and as a rule are confined to the blossom 
end of the fruit although they may occur on the sides or on the stem 
end. Affected apples may be dwarfed and deformed. 

On the twigs 

In apples of very susceptible varieties twigs of the current year's growth 
may be severely affected by the rust. Infection takes place early in the 
season. The twig does not elongate, but it increases in diameter, and as a 
result a short, thick, stubby twig is produced in which pycnia and aecia are 
formed in abundance. Seriously affected twigs die at the end of the season. 




FlG. I40. APPLE FRUIT AFFECTED BY GYMNOSPORANGIUM JUNIPEKI-VIRGINIANAE 

The apple on the right shows the aecia protruding from the surface, while the apple on the left 

shows only pycnia 

ETIOLOGY 

Nomenclature 
The cedar fungus was first named Gymnosporangium J 'uniperi-virginianae 
by Schweinitz in 1822. In 1825 it was named G. macropus by Link, 
but G. J uniperi-virginianae is considered the accepted name. 



Life history 
Telial stage 

Inoculation of cedar. — According to Kern (191 1), Plowright was the first 
to infect cedar trees with a rust fungus. On June 25, 1884, he inoculated 
a small one-year-old juniper seedling, about 2.5 centimeters high, with 



5i6 



Bulletin 390 



G. clavariaefornie (Jacq.) DC. Evidence of infection was apparent on 
July 1 but the tree died before any spores were formed. In another 
instance Plowright inoculated a tree 3 decimeters high and spores were 
produced one year from the following spring, showing that nearly two 
years are necessary for the completion of the life cycle of the fungus. 
Heald (1909) failed to obtain infection in cedars with G. Juniperi- 
virginianae. 

Each summer for the past three years, small cedar trees growing in the 
greenhouse have been inoculated by the writer. The methods used in 
making the inoculations were for the most part those employed by Kern 
(191 1) in infecting aerial hosts. Aeciospores were scraped from an affected 
apple leaf into tap water, and the suspension of spores thus obtained was 
sprayed on a cedar tree with an atomizer. Other affected leaves were 
suspended over the tree so that the spores fell directly on it. After the 
tree was sprinkled with the infected water it was covered with a large 
bell glass so that the moisture would be retained. Each day the bell 
glass was removed and the inner surface sprayed with water, in order 
to maintain a moist atmosphere. After a period varying from forty 
to sixty hours the bell glass was removed. 

In the autumn of 19 14 five trees were thus inoculated. The results 
are recorded in table 1 : 

TABLE 1, Inoculation of Cedar Trees with Spores of Gymnosporangium 

JUNIPERI-VIRGINIANAE IN I914 



Number of trees 
inoculated 


Date of 
inoculation 


Number of 
infections 
apparent 


Fungus 


3 


July 25 

September 8 . . 
September 27.. 


1, on July 30, 1915*.. 

No infection 

No infection 


G. Jan ipen-virginianae 


1 


G . Jim iperi-virginia nae 


1 


G. Junipcri-virginianae 









* See discussion of this case in the text, page 517. 

All the inoculated trees were examined carefully on November 6, 1914, 
but no sign of infection was evident. In one case certain parts of several 
leaves were yellowish green in color, closely resembling infected leaves, 
but there was no further development and the leaves finally died. On 
July 26, 19 14, two cedar trees which had been inoculated with G. Juniperi- 
virginianae the previous autumn showed certain leaves that appeared 
to be infected. Leaves on different stems showed yellow discolorations, 
while, the other leaves were of the normal green color. Although the 
leaves with the discolored spots died without showing further evidence 



Three Cedar Rtst Fungi 517 

of infection, it is possible that the fungus was more virulent under these 
conditions and killed the leaves without showing any signs of gall develop- 
ment. None of the foliage on the check trees showed the yellow 
discoloration. 

On July 30, 191 5, a small cedar apple was found on a cedar tree that 
had been inoculated on July 25, 19 14, by suspending over the tree the fruit 
of an apple infected with G. Juniperi-virginianae. When first observed 
this gall was one millimeter in diameter, globose, and green in color. 
It appeared to be developing from the upper, or inner, side of a small 
scale leaf. This tree was brought into the greenhouse in the early spring 
of 19 1 4 and all cedar apples were removed. It was carefully examined 
again on April 10, 191 5, for any signs of cedar apples and none were found. 
That this gall could have been the resitlt of natural infection before the 
tree was removed to the greenhouse seems impossible, since in that case 
it would have developed in the previous year. The gall was undoubtedly 
that of 67. Juniperi-virginianae, as is evident by its method of origin, 
its color (at first green and later turning to the characteristic brown), 
and its surface character. By October 1 it had doubled in size, and spores 
were produced in February of 1916. Apparently the gall resulted from 
the inoculation. It is, however, impossible to determine this point 
absolutely. 

Susceptibility of individual trees. — Observations made during the past 
three years seem to indicate that individual cedar trees show a difference 
in susceptibility. Some may be severely affected while others are 
practically free from the disease. Certain trees produce a considerable 
number of G. J uniperi-virginianae galls, while others bear almost exclusively 
the galls caused by G. globosum, and still other trees may be affected 
severely by G. clavipes. Furthermore, some of the trees may have all 
three species present in great abundance, but usually a tree is attacked 
primarily by a single species. 

There is a wide variation in the number .of cedar galls of G. Juniperi- 
virginianae produced from year to year. This variation usually depends 
on the abundance of the alternate stage in the preceding year. This 
is not always true, however, since favorable infection weather may not 
prevail at the time when infection of the cedar would naturally occur. 
In the summer of 19 14 an abundance of the aecial stage of all three species 
was produced, and a corresponding increase in the number of cedar apples 
was apparent in the fall of 191 5. There is less fluctuation in the case 
of G. globosum and G. clavipes, since these forms are perennial. 

Injection period. — It is generally accepted that infection of the cedar 
may occur with the production of the first mature aeciospores, and continue 
throughout the season. During the seasons of 191 5 and 1916 the aecio- 



5 iS Bulletin 390 

spores matured about August 1 in New York State. Many workers have 
had difficulty in germinating these spores, and for that reason Reed and 
Crabill (191 5) have advanced the theory that a rest period is necessary 
and that the aeciospores do not germinate until the spring following 
their dispersal. It is probable that the mycelium develops within the 
tissue of the cedar for a period of several months after infection occurs, 
before any material change is noticeable. The galls first make their 
appearance in the latter part of July and continue to grow rapidly until 
late autumn, when they are practically mature. 

Mycelium and haustoria. — Prior to the formation of telial horns, the 
mycelium is distributed throughout the gall, where it occupies the inter- 
cellular spaces. The entire leaf from which the gall originates is per- 
meated with mycelium even before much hypertrophy or other change 
becomes evident. The mycelial cells vary in length and the septa are 
often difficult to locate. This fact undoubtedly accounts for the mistake 
of Sanford (1888) in thinking that no cross walls exist. The binucleated 
condition can readily be demonstrated. The hyphae vary in width but 
average about 2.5 m- 

Haustoria are present, but not abundantly in the voting galls. Reed 
and Crabill (191 5) give a detailed account of the formation of haustoria. 
They were able to find only the very early stages in the autumn, and 
believe that mature haustoria are not developed until just preceding 
teliospore formation in the spring. 

Development of telial horns. — About the first of October or later, 
depending on the season, aggregates of mycelium are developed in certain 
areas, forming typical stromatic layers. The host cells in these regions are 
1 it'ten completely insulated and very small. The rapidly forming mycelium 
inhibits the growth of the host cells in its midst, but the adjoining cells 
continue to multiply and enlarge so that a depression results. From 
these stromatic layers the teliospore stalks arise. Sections of galls collected 
early in December, 1915, show the spore stalks and the immature spores 
in abundance. The spores are cut off from the tips of the short stalk- 
cells by septa, and almost simultaneously become two-celled. The 
young spores contain two nuclei in each cell, but these fuse when the 
spores reach maturity. 

In 191 5 the more advanced galls showed the telial depressions about 
October 1. No further change was noticed until early in the following 
spring, when the telial horns pushed out from the depressions and con- 
tinued to develop for some time. The telial horns consist of a vast number 
of spores borne on much elongated pedicels. They are first formed beneath 
the epidermal tissue, and when warm weather begins the pedicels elongate 
and carry the spores out with them. In 1914 the telial horns began to 



Three Cedar Rust Fungi 519 

make their appearance about the middle of April, and mature spores 
were present on April 25 but gelatinization did not take place until May 5. 
In 191 5 the epidermis was broken open about April 15 and the first 
gelatinization took place on May 8. 

An experiment was conducted to determine whether or not the telial 
horns are capable of gelatinization as soon as they emerge from the gall. 
A cedar apple with horns not more than one millimeter in length was placed 
in a glass beaker containing water. Within less than half an hour the 
horns had swollen to twice their original size. Apparently the spore 
stalks are capable of gelatinization as soon as they have ruptured the 
epidermis of the gall, but an attempt to germinate the spores at this time 
failed. 

The telial horns may become from 2 to 20 millimeters in length by 
1.5 to 3 millimeters in width before the first gelatinization takes place. 
At this time the telial horns are cylindric-acuminate in shape. Thev 
are golden brown in color and are evenly distributed over the surface of 
the gall. With the first warm spring rains after the horns are protruded, 
they enlarge to as much as three times their original size. The horns 
during this period are of a jelly-like consistency and are much lighter in 
color than before, due to the fact that there is less coloring matter in the 
gelatinous spore-stalks than in the spores. With the return of drier con- 
ditions the horns regain approximately their original size. The tips of 
these protrusions usually dry down more than the remainder, and are 
often of a hard consistency. After each succeeding rain one-half hour or 
more in duration, gelatinization may occur, and this may be repeated as 
many as fifteen or twenty times. Nevertheless, some of these periods 
may not be of sufficient duration to permit the spores to germinate. In 
1 9 14 the first gelatinization took place on May 5, and after the horns had 
dried it was noted that for nearly one-fourth of their length from the 
apex to the base they were lighter-colored and much firmer in consistency 
than before gelatinization. After the rain period of May 2 1 about one-half 
of the horn was lighter-colored, and after the rain on June 5 only a small 
area at the base retained its original color and its ability to gelatinize. 
This basal part became swollen on two subsequent occasions, a smaller 
part each time, until finally the horn was light in color throughout and 
became detached from the gall on July 1. 

A microscopical examination of the part of the horns which assumed a 
lighter color showed that approximately fifty per cent of the spores had 
germinated. It has been observed also that the spore stalks of germinated 
spores are unable to gelatinize. They become dry and hard, so that when 
they are teased apart and examined the empty spore walls are generally 
broken from their stalks or only short pedicels remain. It would seem 



5->o Bulletin ^go 

from the foregoing observations that the horn becomes lighter in color and 
hard progressively from the apex to the base, and also that the spores at 
the apex are older, mature earlier, and germinate more readily than 
those at the base. Reed and Crabill (19 15) are of the opinion that the 
teliospores on the outside of the tentacle germinate first and shrivel away, 
and then those on the interior of the tentacle come to the surface and 
germinate in their turn. The writer's observations show that, although 
the spores over the entire surface of the horn germinate, those at the apex 
germinate more readily. These observations agree with those of Wornle 
(1894), who states that the spores at the apex are the oldest. 

Teliospore germination . — The time of spore germination varies with the 
season. In 191 4 and 191 5 the spores were mature about April 25. Tests 
made show that the spores will not germinate as soon as the horns rupture 
the epidermis of the gall. Weather conditions are an important factor, 
and as much as two weeks may intervene before germination occurs. 
When cedar apples with telial horns that were just emerging were brought 
into the laboratory, the spores germinated after about seven days. 

The teliospores are characteristically two-celled, but occasionally one- 
celled and three-celled spores are found (fig. 141, a). They range in width 
from 15 to 22 ix and in length from 33 to 65 ^t. 6 The spore is narrowly 
ellipsoidal to rhombic oval in shape. It is slightly or not at all con- 
stricted at the septum. The wall is cinnamon brown in color and averages 
about 1 n in thickness. The pedicels are thin and of equal diameter through- 
out, varying in width from 3 to 5 fx for different spores. There are two 
germ pores in each cell of the spore, one on each side of the cell near the 
septum. Spore germination is of the usual rust type, resulting in the 
formation of a promycelium bearing four basidiospores (fig. 141, b). 

Heald (1909) found that under favorable conditions the promycelium 
and basidiospores may be produced in from twelve to twenty-four hours; 
Coons (19 1 2) states that the process of developing germ tubes requires 
from six to fifteen hours; while Reed and Crabill (191 5) found four hours 
to be the minimum time for germination. The writer has obtained mature 
basidiospores within less than three hours under optimum conditions; 
in fact, under such conditions from three to four hours is the usual time 
required. 

The most satisfactory germination of teliospores was obtained from 
spores placed on a clean slide in a film of tap water. The slide was placed 
in a petri dish, which contained a small quantity of water to prevent too 
rapid evaporation from the slide. On one occasion a spore taken from a 
telial horn just brought in from the field on a clear day and germinating 
under the conditions described above, had formed a small bud-like process 



6 Spore measurements were made in all cases with an oil-immersion lens, using fresh spores mounted 
in water. 



Three Cedar Rist Fungi 



521 



at the end of one hour; after two and one-half hours the promycelium 
had continued its development and the septa were visible; by the end of 
three and one-half hours the basidiospores were formed. Instances have 
'been noted in which the spores germinated and the basidiospores were 
present within less than three hours. 

One of the important factors affecting spore germination is the amount 
of moisture. Blackmail (1903) discusses this subject in some detail. 
He used spores of other species of rust, placing some in hanging drops 




Fig. 141 . spore forms of gymnosporangium juniperi-virginianae 

A. Various types of teliospores of G. Juniperi-virginianae. x 350. B, Various 
stages and types of teliospore germination of G. Juniperi-virginianae. X 350. 
C. Teliospore of G. Juniperi-virginianae, showing the appearance of the cell con- 
tents when incubated at 30 C. for four hours. x 375. D, Various stages of 
basidiospore germination of G. Juniperi-virginianae. X 350. E, Penetration 
of a basidiospore of G. Juniperi-virginianae directly through the wall of an 
epidermal cell. X 350 



and some on slides in petri dishes. He found that those in hanging drops 
developed long germ tubes and formed no basidiospores until they had 
grown through the drop into the air, which rarely happened. The others 
formed basidiospores and a characteristic promycelium at once. Blackmail 
concludes that the presence or absence of air is the determining factor, 
as this varies with the water supply. 



522 Bulletin 390 

It has often been observed by the writer that teliospores germinating 
on a slide prodtice only long tubes when covered with water, but when 
there is only a small amount of water present the usual promycelium and 
basidiospores are formed. An attempt was made to germinate teliospores- 
in a saturated atmosphere without permitting the spores to come into 
contact with other moisture than that in the atmosphere. This attempt 
failed, but in cases in which the air became supersaturated, and small 
droplets condensed on the slide, germination was obtained. 

Temperature is another factor that plays a large part in spore germi- 
nation. Reed and Crabill (191 5) found that 15 C. was the optimum 
temperature for spore germination and n.5 C. was the minimum. The 
upper thermal death point was 30 C; the lower thermal death point 
was not determined, but it was much below freezing. 

Considerable work has been done by the writer in an attempt to deter- 
mine the most favorable temperature conditions for germination with 
the three rust species studied. For the first of these experiments the 
following method was used: Telial horns were placed in a watch glass 
in tap water and teased apart until several spores could be obtained in 
each drop of water. Suspensions of spores thus prepared were placed 
on slides in petri dishes and allowed to germinate at different temperatures. 
It was found after several trials that spores which had been broken entirely 
free from the horn or were isolated from all other spores did not germinate 
so readily as did those that remained clinging in groups. After repeated 
trials it was found that a better indication of spore germination could 
be obtained by placing a telial horn, or a part of one, on a slide. In 
this way more nearly normal conditions were maintained, but the larger 
number of spores made it impossible to estimate the percentage of germi- 
nation except in a comparative way. In the case of G. J uiii peri-virginianae 
an entire telial horn was placed on a slide, and often horns from the 
same gall were used in a series of tests. In the case of the other two 
species only parts of the horns were used. The quantity of basidiospores 
lying along the side of the horn on the slide was often used as a guide 
in estimating the relative amount of germination. Observations were 
usually made every hour, and the rate of germination for the entire period 
was considered in making the final comparisons. 

The extremes found for all three species were practically the same 
as those found by Reed and Crabill (191 5) for G. Juniperi-virginianae, 
the lowest temperature at which germination occurred being 7 C. and 
the highest 29 C, with the upper thermal death point 30 C. (fig. 142). 
The optimum temperature, however, as shown by these experiments, 
ranges from 22 to 25 C, the best germination taking place at from 
23 to 2 4 C. These experiments were run in triplicate and were repeated 
on several occasions throughout the season, so that some temperatures 



Three Cedar Rust Fungi 



5 2 3 



were tried at least twelve times. In all cases the results obtained were 
uniform. Reed and Crabill (191 5) found that a temperature above 
20 C. greatly retarded the development of basidiospores and that no 
spores were produced when the temperature was above 24 C. In the 
writer's experiments an abundance of basidiospores were obtained at a 
temperature ranging from 22 to 25 C, and there were some at 2 6° C. 
After incubating at 30 C. no spores germinated, even when placed under 
optimum conditions. The oily contents of the spores coalesced into 
large drops, giving the appearance shown in figure 141, c (page 521). The 
normal variation is relatively great in tests of this kind, but the exper- 
iments were repeated a sufficient number of times to make the obser- 
vations comparatively conclusive. 

Very good - 



Medium - 



Fair - 



None 




FlG. I42. INFLUENCE OF TEMPERATURE ON GERMINATION OF RUST SPORES 

The curve shows that the best germination of teliospores occurred at a temperature 
between 22° and 24 C. 



When conditions arc unfavorable for germination a long germ tube 
may be formed or a bud-like process may take the place of a promyeelium. 
Again, the promyeelium may break up into four parts, each of which 
may then form a basidiospore or may germinate by a germ tube. The 
cells of the promyeelium may germinate by germ tubes without breaking 
apart, or other uncommon methods of germination may occur. These 
abnormal conditions of germination are usually found where an over- 
abundance of moisture is present or where the temperature is somewhat 
lower than the optimum. 

Dissemination of basidiospores. — When the basidiospores reach maturity 
they are forcibly discharged from their sterigmata. With the beam-of- 
light method the falling of basidiospores was observed by the writer in 
the same manner as is described by Buller (1909) and later by Coons 



5_>4 Bulletin 390 

(1912). An experiment was set up in which the discharge of basidiospores 
began at half past six o'clock in the evening of one day and continued- 
until after ten o'clock the next forenoon — although at that time the 
rate of discharge was much slower. Evidently the dispersal of hasidio- 
spores can continue for some time after a period of rainfall if slow-drying 
conditions prevail. In observing the process under the microscope an 
abrupt sidewise movement of the basidiospore was always noticed several 
seconds previous to its discharge, and almost simultaneously a bubble 
appeared at its base. 

The basidiospore farthest from the spore is the first to be formed, followed 
by the others in their respective order. The outermost spore is discharged 
first, followed by the next in order. Only about one minute elapses 
between the disappearance of the apical basidiospore and the one nearest 
it, but a much longer period elapses before the last two are discharged. 
Often the terminal basidiospore is mature before the sterigma of the 
basidiospore nearest the spore is even formed. This method of discharge 
readily accounts for the wide dissemination of basidiospores by air currents. 

Germination of basidiospores. — Farlow (1886), Crabill (1913), and 
Reed and Crabill (191 5), have contributed to the knowledge of secondary 
basidiospore formation. The basidiosp< >re normally germinates by the 
development of one or more, rarely two, germ tubes from the side of the 
spore. Under certain conditions, instead of a germ tube a sterigma 
similar to those formed on the promycelium is put forth, and on the end 
of this a secondary basidiospore is produced. This secondary spore is 
identical in appearance with its parent except that it is somewhat smaller. 
Various stages of basidiospore germination are seen in figure 141, d 
(page 521). The chief factor influencing the production of the secondary 
spore is an excess of moisture. 

Two cedar apples, one caused by G. Juniperi-virginianae and the other 
by G. globosnni, with horns protruded, were subjected for twelve hours 
to a fine mist from a spray nozzle attached to a water tap. The tem- 
perature of the room was 23 C. and that of the water about 8° C. When 
the material was examined it was found that a large number of the spores 
had germinated abnormally, and that the basidiospores which were 
formed had already germinated by means of secondary spores. It is 
impossible to determine whether or not the excess moisture was the only 
cause of this abnormal germination, since the temperature factor may also 
have been of importance. 

Aecial stage 

Inoculation and infection of apple. — The first basidiospores are usually 
disseminated in the spring about the time when the buds of the aecial 
hosts open, though some may be formed previous to this time. Infection 



Three Cedar Rust Fungi 1525 

usually occurs on the dorsal surface of apple leaves. The germ tube 
penetrates the epidermis and the pathogene becomes established within 
the tissues of the host. 

In these inoculation experiments a suspension of basidiospores in tap 
water was placed on various parts of both the upper and the lower surface 
of Wealthy apple leaves. After seven, fourteen, and twenty-one hours, 
respectively, parts of the leaves thus inoculated were removed, fixed, 
and embedded in paraffin. Several of these were later sectioned and 
examined. In one case, after a period of seven hours a germ tube of 
a basidiospore was found to have penetrated the lower epidermis directly 
and passed about two- thirds of the distance through the epidermal cell 
(fig. 141, e, page 521). 

Several leaves from a small apple tree were inoculated by placing 
basidiospores in suspension on the foliage, with a camel's-hair brush. 
Some leaves were inoculated on the upper surface and others on the 
under surface. Infection was apparent after ten days on all the inoculated 
leaves. This demonstrates that infection can take place on either the 
upper or the lower surface of the leaf. In all cases, however, pyenia 
were produced only on the upper surface. Apparently, therefore, the 
production of pyenia on the upper surface of infected leaves is due, 
not to the fact that infection occurs there, but to some other factor. 
Pyenia have never been seen on the lower surface of leaves, although 
many aecia have been observed arising vertically from the upper surface. 

In 1 9 14, and also in 19 15, the first evidence of infection' in nature was 
found about June 1. The mycelium is similar to that found in the telial 
hosts except that it is uninucleate and only a limited area of the host 
tissue is invaded. 

Effect of environmental factors. — It is evident that the amount of rust 
present in a given season will depend largely on weather conditions. 
Moisture is necessary for teliospore germination and for infection of the 
aecial host, and therefore the number of infection periods depends primarily 
on the number of rain periods. 

An attempt was made in these experiments to determine the approxi- 
mate amount of moisture necessary for infection of the aecial host. Cedar 
apples were immersed in tap water for a few minutes and were then 
placed under a bell glass. After about four hours, when an abundance of 
basidiospores were being discharged, the gall was suspended over a small 
apple seedling. A lamp chimney inclosed both the seedling and the gall. 
The seedling was not moistened. The cedar apple retained its moisture 
for a long time in this position, and the basidiospores formed a yellow 
coating over the surface of the leaves of the seedling within a few hours. 
After eighteen hours the chimney was removed, and ten days after inocu- 
lation abundant infection was evident on nearly all the leaves. This 



526 Bulletin 390 

experiment was repeated several times and in each case the same results 
were obtained. Apparently sufficient moisture collected on the leaves 
from the water transpired and from that which evaporated from the 
telial horns to permit basidiospore germination and infection. A careful 
inspection failed to disclose any drops of water collected on the leaves 
inside the chimney. 

Other experiments were attempted in which the lamp chimney con- 
taining the cedar apple was suspended over the apple tree so that the 
basidiospores fell on the tree but no opportunity was offered for the con- 
densation of water on the leaves. No infection occurred under these 
conditions. This experiment was repeated on a large tree in the open. 
The basidiospores were allowed to fall on a few young leaves which were 
not inclosed within the chimney. On the night when the experiment 
was set up there was a heavy dew followed by forty-eight hours of precipi- 
tation. Abundant infection occurred and aecia were developed within 
the usual period of time. 

From these experiments it is evident that but little moisture is neces- 
sary for infection. There must be sufficient moisture to cause the telial 
horns to gelatinize and to keep them in that condition for a period of 
from four to five hours, followed by conditions of high humidity to furnish 
the necessary moisture for infection. This is contrary to the opinion of 
Reed and Crabill (1915), who state that infection takes place only in the 
presence of abundant moisture. It is not clear whether they mean 
to include the whole process of basidiospore formation and infection or 
only the latter, since they also make the statement that infections followed 
short periods of rainfall. 

Strains of the jungns. — Since this disease is so destructive in West 
Virginia and Nebraska, specimens of cedar apples from each of these States 
were procured for the purpose of making comparative inoculation * tests 
with the strain of the fungus found in the vicinity of Ithaca, New York. 
These specimens, obtained through the kindness of N. J. Giddings and 
E. M. Wilcox, were used to inoculate Wealthy apple trees in the open 
and apple seedlings in the greenhouse. Young leaves on different branches 
of each tree were inoculated with the three strains of fungi and their 
development was observed closely. Infection was apparent at exactly 
the same time in all cases and the development of the disease was identical 
in all particulars. In no case was there any evidence to show that one 
strain was more virulent than the others. The apples of West Virginia 
and of Nebraska may be more susceptible than those of central New 
York, which probably accounts for the fact that this disease is so destructive 
in the former States. 

Varietal susceptibility of apple. — Numerous lists of susceptible and of 
resistant varieties of apples have been recorded by various writers. The 



Three Cedar Rust Fungi 



527 



most important of these are by Emerson (1905) in Nebraska, Chester 
(1896) in Delaware, R. E. Stone (1908) in Alabama, Smith and Stevens 
(1910) in North Carolina, Reed, Cooley, and Crabill (1914) in Virginia, and 
Giddings and Berg (19 15) in West Virginia. Stewart (1910) says that in 
New York State the varieties Wealthy. Boiken, and Rome are very 
susceptible, Hubbardston and Sutton arc slightly susceptible, and 
Mcintosh, Yellow Transparent, Gravenstein, Red Astrachan, Olden- 
burg, and Baldwin are resistant. The writer has had no opportunity to 
make observations on the susceptibility of different varieties of apples, but 
the following have been artificially infected several times: Wealthy, Wag- 
ener, Twenty Ounce, Tompkins King, Alexander, Baldwin, Rome Beauty, 
Bietigheimer, Baxter, Boiken, Banana. Black Gilliflower, Dartmouth. 




Fig. 143. pycnium of gymnosporangium globosum in Crataegus 

LEAF. X 350 

The variety Wealthy is considered especially susceptible, although 
Stewart and Carver (1896) state that it proved, to be resistant in Iowa. 
Seedling apples are very susceptible when artificially inoculated. 

Several specimens of Salome apples were received in the autumn of 
1 913 and a large rust lesion was present on the blossom end of each. 
This variety should probably be included with those listed as susceptible 
in New York State. 

Pycnia. — The pycnia are the first fruiting bodies to appear in apple 
tissue attacked by the rust fungus. Masses of short-celled mycelium 
collect at certain points under the epidermis and form the flask-shaped 
pycnia of the usual rust type. Hyphal branches extend into the pycnial 
cavity and from the ends of these the pycnospores are abstricted (fig. 143). 



528 



Bulletin 390 



Aecia. — From two to four weeks 
after the pycnia become visible, de- 
pending largely on weather conditions, 
the aecia begin to break out on the 
lower surface of the leaves or from 
among the pycnia on stems or fruit. In 
New York State the aecia usually begin 
to break open about the first of August. 
The tissues from which these fruiting 
bodies arise may be considerably hyper- 
trophied, the spongy parenchyma .espe- 
cially being modified. Many septate 
strands of mycelium collect beneath 
the surface in the diseased area and 
from these the aecia are finally developed. 
The aecia are formed entirely within 
the host, but as they mature they 
break through the inclosing tissue, the 
peridium soon dehisces, and the spores 
are then scattered. 

The aecia in all cases are composed of 
the inclosing pseudoparenchyma, the 
fertile spore-bearing stalks, and the 
aeciospores surrounded by the single 
layer of peridial cells (fig. 144). The 
aecia spores are binucleate and measure 
16 to 24/i by 21 to 31 ju- The spore 
wall varies in color from yellow to 
brown. When dehiscence occurs the 
peridium splits longitudinally between 
practically each row of cells. The ends 
of the cells remain attached, forming 
long strands which are one or more 
cells wide by several cells long. The 
individual cells are comparatively long 
and narrow, measuring 10 to 16 /j. by 
65 to 100 m; they become much re- 
curved when moist. The side walls 
are sparsely rugose with ridges extend- 
ing the entire distance across. The 
aeciospores drop out of the aecia as they 
mature, and are carried by the wind 
to cedar trees where they initiate the telial stage. 




Fig. 144. aecium of gymnosporan- 
gium globosum in crataegus 

LEAF 



Three Cedar Rust Fungi 



529 



Germination of aeciospores. — Many investigators have experienced 
great difficulty in germinating aeciospores. Heald (1909) states that 
he succeeded in germinating them previous to the first of October, after 
which time only one or two per cent germinated. Reed and Crabill (191 5) 
found it impossible to germinate them except for an occasional germ 
tube, which seemed to be in a very weakened condition. Numerous 
trials made by the writer indicate that only a small proportion of these 
spores are capable of germination. 



TABLE 2. Results of Aeciospore Germination Tests of Gymnosporangium 

JUNIPERI-VIRGINIANAE IN I915 



Num- 










Percent- 


ber 

of 


Date 


( Cultural 
solution 


Temper- 
ature 


Method 


age of 
germi- 


slides 










nation 


5 


August 5 . . 


0.2 per cent cane 
sugar and 
cedar leaf 


24 C. .. 


Spores on dry slide, 
culture solution 
added 


1 


1 


August g 


0.2 per cent cane 
sugar 


24 C 


Spores on dry slide, 
culture solution 
added 


75 


1 


August 5 


0.2 per cent cane 

sugar 


24 C. 


Spores on dry slide, 
culture sol ui mi i 
added 


25 


3 


August 5 


0.2 per rent cane 
sugar 


24 C.. 


Spores on dry slide, 
culture solution 
added 





5 


August 5 


Tap water 


24 C . . . . 


Spores on dry slide, 
culture solution 
added 


1 


2 


August 5 


0.2 per cent cane 
sugar 


24 C. 


Spores shaken on 
slide, culture solu- 
tion sprayed in 
fine droplets on 
slide 





5 


August 5 


0.2 per cent cane 
sugar 


24° C... 


Spores shaken on 
slide, small drop 
of solution added 





5 


August 5 


0.2 per cent carie 


24 C.... 


Large drop of solu- 


2 spores 






sugar 




tion placed on 
slide, spores 
allowed to fall 
on solution 


on each 
slide 


2 


September 29 


Tap water 


22° C. . . . 


Suspension of 
;pores 





1 


September 29 


Tap water 


23° C... 


Suspension of 
spores 





1 


September jg 


Tap water 


26 C . . . 


Suspension of 
spores 





4 


September 29 


Tap water 


15° C. 


Suspension of 

5] >< >rcs 





2 


August 28 


Tap water 


23 C. 


Spores shaken on 
dry slide, then 
placed in moist 













chamber 





530 Bulletin 390 

The method used in this work was practically the same as that recorded 
for the germination of teliospores. Water and a cane-sugar solution 
were used as culture media, to which, on various occasions, cedar leaves 
were added. In some cases the spores were shaken directly on the slide 
in order to obtain only mature spores, while in other preparations the 
aecia were placed on the slide and crushed, thus liberating all the spores 
present. The quantity of culture solution was varied, and in some cases 
the spores were first placed on the slide and the culture media was then 
added, while in other cases the spores were allowed to fall onto the surface 
of the culture solution. 

The results of these experiments are recorded in table 2. Apparently 
a small proportion of aeciospores germinate under artificial conditions. 
Some of the spores used in the experiments were obtained from naturally 
infected and others from artificially infected leaves. The presence of cedar 
leaves in the culture media did not influence the germination of the spores. 

Other germination tests were made with spores used for inoculating 
cedar trees, but only a few spores germinated. Hanging-drop mounts 
were employed in some cases not recorded, but these yielded no better 
results. 



Three Cedar Kust Fung 



533 



THE DISEASE CAUSED BY GYMNOSPORANGIUM GLOBOSUM 

The disease caused by the fungus Gymnosporangium globoswm is com- 
monly known as cedar rust, Crataegus rust, or pear rust, depending on 
the stage referred to. 
The pathogene is native 
to North America and 
was first studied care- 
fully by Farlow (1880). 
It is widely distributed 
throughout the eastern 
section of the United 
States, where it causes 
a rust of various species 
of Crataegus. The dis- 
ease is of little eco- 
nomic importance, al- 
though on rare occa- 
sions the fungus attacks 
pears and quinces 
• (Stewart, 10 to). 

symptoms 
On cedar 
The galls produced 
by this species are sim- 
ilar in appearance to 
those caused by G. Ju- 
niperi-virginianae. The 
gall produced by G. 
globosum, as the name 
would indicate, is usu- 
ally globose in shape 
and is not so large as 
the gall caused by G. Ju- 
niperi-virginianae. The 
surface of the young 
gall in early autumn is 
smooth except for the 
shreds of the old leaf which cling to it. It approaches mahogany red in 
color, in contrast to the greenish brown of the G. J uui peri-virginianae 
gall. Instead of the pit-like depressions on the surface, the galls pro- 




Fig. 145. 



CEDAR APPLE CAUSED BY GYMNOSPORANGIUM 
GLOBOSUM. WINTER CONDITION 



S3 2 



Bulletin 390 



duced by <. : . globosum have small elevated areas, or mounds (fig. 145). 

From these raised areas the telial horns appear in the following spring. 
The telial horns are wedged-shaped and are chestnut brown in color 

dig. 146). Scars of the horns of former seasons are often apparent 

between the horns on 
old galls. When the 
warm spring rains occur, 
the protrusions gelati- 
nize and enlarge to 
about double their nor- 
mal size (fig. 147). These 
horns dry and drop off 
at the end of the fruit- 
ing season, but the galls 
may continue to live 
and bear spores for 
several seasons. The 
old galls turn brown 
and become roughened 
on the surface due to 
the scars of the telial 
horns. 

On quince 
A yellow spot, such as 
rharaeterizes the lesions 
caused by G. Juniperi- 
virginianae on the apple 
leaf, is formed by 67. glo- 
bosum on quince foliage. 
The pyenia and the aecia 
are likewise formed on 
the upper and the lower 
surface of the leaf, re- 
spectively. To all ex- 
Fig. 146. gall caused by gymnosporangium globosum t e rnal appearances the 

The typical telial horns are shown prior to gelatinization 

symptoms are the same 
as those described lor G. Juniperi-virginianae on apple foliage. 




( hi pear 
Stewart (1910) states that infected spots on the upper surface of pear 
leaves are dark brown or nearly black in color, with a conspicuous red 



Three Cedar Rx t st Func.] 



border. Spots on the under surface arc of the same dark color but have 
no red border. Aecia are produced in the largest lesions and also on 
the infected leaf petioles. In many cases the rust spots arc arranged in 




FlG. 147. TELIAL HORNS OF GYMNOSPORANGIUM GLOBOSUM FULLY 
GELATINIZED 

two irregular rows, one on each side of the midrib, giving the appearance 
of infection having occurred before the leaves were unfolded. In 19 10 
Stewart observed that infected fruits were still clinging to the trees on 
June 15, although they were usually less than half the normal size. The 



534 



Bulletin 3 00 



fruit is often deformed and bears a circular, flattened, black lesion devoid 
of aecia near its base. Aecia are produced rarely. 



On Crataegus 

The lesion produced by G.. globosum on Crataegus leaves is almost 
identical with the rust lesions on apple foliage. The red border about the 
margin of the spot is not so common, however, and the aecia are rarely 
arranged in the form of a circle (fig. 148). 

The twigs of Crataegus are not commonly affected by this rust, but 
an occasional twig infection has been observed. The lesion is yellow, 




FlG. I48. CRATAEGUS LEAF ARTIFICIALLY INOCULATED WITH 
GYMNOSPORANGIUM GLOBOSUM 

The groups of pyenia are apparent in the lesions 

similar to that on the leaf, but practically no swelling of the t\vi^ r is 
apparent. Pyenia are produced in this discolored area, followed later 
by aecia (fig. 149). 



Thrkk Cedar Rust Fungi 



535 



Infected fruits have been found, but these are not common. Here 
again a yellow spot is formed but little or no hypertrophy results. The 
pyenia and the aecia follow in the same lesion. 




Fig. 149. aecia of gvmnosporangium globosum 

The aecia arc developing from the under surface of Crataegus leaves. The stem 
and the leaf petiole are also affected 



ETIOLOGY 

Nomenclature 
The fungus now known as G. globosum was first named by Farlow in 
1880. He gave it the name G. fuscum var. globosum, but later (Farlow, 
1880) changed the name to G. globosum. 

Life history 
The details of the life cycle of this species are almost identical with 
those of G. Juniperi-virginianae. The aeciospores of the two species 
mature at approximately the same time. The time of infection of the 
cedar has not been determined, but it is presumably during the period 
when the aeciospores are being dispersed. 



536 Bulletin 390 

Rust-infected Crataegus leaves were collected on September 26, 1914, 
and exposed to the weather in a wire screen. At this time aeciospores 
taken from these leaves failed to germinate. Subsequent tests were made 
and germination was obtained until December 15, but all attempts to 
germinate these spores after this date failed. 

Since aeciospores will germinate during and even later than the time 
of their dispersal, the writer sees no reason for assuming that infection 
does not take place until the following spring, as Reed and Crabill assume 
for G. Juniperi-virginianae. Although the penetration of the germ tube 
has never been observed, there is but little doubt that it enters the stomata. 
The mycelium develops within the cedar leaf for a period of from ten to 
twelve months before any sign of infection becomes apparent. 

Telial stage 

Development of telial horns. — The mycelium of this species is practically 
identical with that of G. Juniperi-virginianae and there is almost a com- 
plete absence of haustoria in the young galls. The telial horns are 
developed from a stromatic layer in the same manner as are those of 
G. Juniperi-virginianae. They begin to develop in the autumn but it 
is not until early the next spring that they become far enough advanced 
to penetrate the surface of the gall. 

In the spring of 191 5 the epidermis over the papillae had begun to 
break open on March 29, while at that time no evidence of this breaking 
could be found on the galls of G. Juniperi-virginianae. The telial horns 
were apparent on April 10. No growth in plant life was evident at that 
time and there was still considerable ice and snow on the ground. Spores 
capable of germination were present in these tentacles on April 15. 

The telial horns continue to increase in size so that when gelatinization 
first takes place they may be from 1.5 to 3 millimeters thick by from 2 to 5 
millimeters broad at the base and from 6 to 12 millimeters high. The 
number of horns on a gall varies from one to one hundred or more. They 
are distributed on the gall unevenly and are chestnut brown in color. 
Instead of standing singly they may coalesce and form a continuous band 
around the gall. The horns of G. Juniperi-virginianae have never been 
seen to fuse in this way. 

The first gelatinization period usually coincides with the first warm 
rain period after the horns are protruded, and the number of times this 
process may occur during a season varies greatly. In 1914 the horns 
gelatinized four times and fell off on May 20, while in 1915 twelve such 
periods were recorded before the horns became dry on June 2. 

The telial horns of this species may be more than double in size when 
swollen, and are then thinner in consistency than the iellv-like horns of 



Three Cedar Rust Fungi 



537 



67. Juniperi-virginianae under similar conditions. After each protrusion 
the horns of the latter species dry down to their normal form with the 
exception of the tips. In the case of G. globosum drying occurs until the 
last gelatinization takes place, at which time the horns form a solid mass 
of thin, jelly-like substance over nearly the entire surface of the gall, and 
this substance intermingles with the adjoining leaves and twigs. When 
drying occurs this material clings to the leaves or twigs and is pulled 
loose from its attachments. The galls do not die as do those of the other 
species, but live and fruit year after year. 

The teliospores of G. globosum closely resemble those of 67. Juniperi- 
virginianae. They are practically of the same width, from 15 to 21/1, 
but are often somewhat shorter, ranging in length from 37 to 54 yu- There 
are also the same number of 
pores and these are similarly 
located. The spore stalks are 
cylindrical in form. Teliospore 
germination is similar to thai of 
G. Juniperi-virginianae (fig. T50). 





Pig. 



I50. VARIOUS TYPES OF TELIOSPORES 
OF GYMNOSPO&ANGIUM GLOBOSUM 



Aecial stage 

The pycnia and the aecia of 
G. globosum are similar to those 
of G. Juniperi-virginianae, the 
greatest difference being in their 
size. The size and shape of the 
peridial cells is somewhat dif- 
ferent for the two species. The 
peridial cells of G. globosum are 
broadly lanceolate in face view 
and measure 15 to 23^ by 60 
to 90 jx, and are linear-rhomboid 
in side view, measuring from 13 to io/x thick. The outer wall is smooth 
and about 1.5 /x thick, while the inner and side walls are slightly thicker 
and are rugose with ridge-like papillae of varying lengths. 

Acciosporc germination. — Most attempts to germinate the aeciospores 
of G. globosum have yielded negative results. On two occasions slight 
germination was obtained, as is shown in table 3. 

Inoculation of cedar trees. — Following the methods described under 
67. Juniperi-virginianae, many attempts have been made during a period 
of three years to obtain infection of red cedar with 67. globosum, but thus 
far no positive results have been obtained. 



Sunn- of the teliospores and basidiospores have germ 
nated. x 350 



538 



Bulletin 390 



TABLE 3. Results <>: Aeciospore Germination Tests of Gymnosporangium 

GLOBOSUM IN 1915 



Num- 










Percent- 


ber 


Date 


Cultural 


Temper- 


Method 


age of 


of 




solution 


ature 




germi- 


slides 










nation 


2 


September 2g 


Tap water. . 


22° (' 


Suspension of 
spores 





2 


September 29 


Tap water 


23' c 


Suspension of 

spores 





3 


September 29 


Tap water. 


15° C. 


Suspension of 
spores 





5 


September 30 


Tap water 


24 C. 


Spores in test tube 
immersed in an 
ice-and-salt bath 
at -4 to -6° C. 
for 1 hour, then 
allowed to in- 
cubate in tap 
water at 24° C. 





5 


October 2 


Tap water 


2 4 °C. 


Spores treated same 
as above but not 
frozen, then sus- 
pended in water 
and incubated at 
-'4° C. 





20 


October 2 


Tap water. 


-4 to 
+28° C. 


Suspension of 
spores 





2 


November X. 


Tap water. 


24° C 


Spores in suspen- 
sion; taken from 
leaves exposed to 
the weather since 
Sept. 26, 191 5 


10 


1 


December 9 


Tap water 


24° C 


Spores in suspen- 
sion: taken from 
leaves exposed to 
the weather since 
Sept. 26, 191 5 


2 spores 
germi- 
nated 
(only a 
few 
spores* 
were 
present 
in this 
mount ) 



Three Cedar Rust Fungi 539 



THE DISEASE CAUSED BY GYMNOSPORANGIUM CLAVIPES 

The rust fungus Gymnosporangium clavipes causes a disease of quince, 
Crataegus, and cedar, which is commonly known as quince rust, Crataegus 
rust, <>r cedar rust. The fungus is native to North America and was first 
studied in some detail by Farlow (1880). It is widely distributed in 
eastern and central United vStates but is of little economic importance 
except on the quince. The writer observed a severe outbreak of quince 
rust in western New York in the summer of 191 2. 

The chief source of loss from quince rust is due to the misshapen or 
stunted condition of the diseased fruit. Twig infections also are common 
and these result in the death of the shoots affected. 

SYMPTOMS 

( ';/ cedar 
On cedar the lesions of G. clavipes arc confined to the twigs, and are less 
conspicuous than those of the other two species herein described. This 
species forms no large pendent galls, and in the early stages, as well as in 
many of the later ones, there is no noticeable hypertrophy of the affected 
twigs (fig. 151). A fusiform swelling may often occur, however, produc- 
ing roughened areas on the bark (fig. 152). The affected areas may vary 
from 1 to' 30 centimeters or more in length, but it is difficult to detect the 
early stages of infection of cedar until the telial sori emerge in the spring 
from the diseased areas. The telial sori are small, hemispheric, and 
orange-brown in color, and may also occur on the young shoots among the 
leaves. They gelatinize in early spring, and, as is true of the two pre- 
ceding species, they finally dry and fall off. The fungus continues to 
fruit from the canker year after year. 

On quince 
Although quince leaves are not commonly affected by G. clavipes in 
nature, infection has been produced artificially on several occasions. 
The veins alone are attacked and often become swollen to double their 
normal size. The swelling of these veins causes the leaves to curl. The 
lesions are not accompanied by a change in color, as is the case with 
infected areas of apple or Crataegus leaves and of quince leaves affected 
by G. globosum. Pycnia are produced in longitudinal rows along the 
affected veins, similar to those described for 67. globosum on pear foliage, 
but no aecia have ever been found. The leaves are finally killed and 
soon fall after the aecia are produced on the stem below. 



5 lo 



Bulletin ^90 



In the spring the terminal buds of quince shoots are often attacked, 
the growth of affected twigs is retarded, and an increase in diameter occurs. 
The foliage is stunted, as in the case of the rust on apples. Pycnia and 




Fig. 151 - Fig. 152 

FlG. 151. CANKER SHOWING TELIAL SORI OF GYMNOSPORANGIUM CLAVIPES 

FlG. 152. CANKER CAUSED BY GYMNOSPORANGIUM CLAVIPES 

The diseased area has a roughened appearance and is slightly enlarged as compared with the stem above 

and below 

characteristic aecia appear later. Affected twigs die at the end of the 
season. On diseased quince fruit the affected part is often much enlarged, 
and in this area pycnia and aecia develop in abundance. 



Threk Cedar Rust Fungi 



54i 



On C 'rataegus 

The symptoms caused by G. clavipes on Crataegus are almost identical 
with those on quince. Although the leaves are rarely attacked, diseased 
leaves become curled and finally die without producing aecia (fig. 153). 




FlG. 155. GYMNOSPORANGIUM CLAVIPES AFFECTING LEAVES, PETIOLES, 
AND STEMS OF CRATAEGUS 

These infections were produced by artificial inoculation 

The stems, the leaf petioles, and the fruit are attacked commonly, and 
hypertrophy of the affected area occurs without change in color. Pycnia 
and aecia are produced in great quantities (fig. 154). The hypertrophied 
area is in some cases confined to only one side of the stem or the fruit. 



542 



Bulletin 390 




Three Cedar Rust Fungi 543 

The thorns are often attacked and enlarge to double their normal size. 
The fungus may extend from an infected thorn into the twig at the base, 
and form a canker in which aecia may be produced in abundance late in 
the season. On October 12, 191 5, a specimen was received from Romulus, 
New York, which bore fresh aecia in a canker that had developed at the 
base of a thorn. 

etiology 
Nomenclature 
This fungus was first named Caeoma (Peridermium) germinate by 
Schweinitz in 1832, and was given the name G. clavipes by Cook and Peck 
in 1873. Since the latter name is the first applied to the telial stage, it is 
the one now commonly accepted. 

Life history 

Only a small amount of literature has appeared which has a bearing 
on the origin and development of the telial stage of G. clavipes. This 
may be due, in part at least, to the fact that the disease causes little or 
no malformation on cedar. 

Judging from analogy with other species, it is assumed that infection 
takes place in the late summer and autumn when the aeciospores are 
scattered; but no evidence of a diseased condition becomes apparent 
until the appearance of the telial sori. The sori develop on the two- 
years-old twigs and are apparently the result of infections of the previous 
year. This is in accordance with the process in the preceding species. 
The incubation period of this species is the same as that for G. globosum 
and G. Juniperi-virginianae; the infections that occurred during the 
summer and autumn of 19 13 did not appear until the spring of 191 5. 
The mycelium, which is similar to that of the other species, collects in 
masses beneath the corky exterior covering of the cedar twig, and from 
these stromata the spores arise and produce the telial horns (figs. 155 
and 156). 

Telial stage 

Development of telial sori. — The first evidence of infection by G. clavipes 
is the appearance of the mound-like telial sori. These were first noticed 
in 191 4 on April 22 and in 191 5 on April 15. In 1914, however, the first 
basidiospores were formed in nature on May 5, while in 19 15 some were 
produced on May 1. The telial sori appear on what seem to be normal 
and healthy twigs (fig. 157). They may be found emerging from the 
bark of branches of all sizes. In most cases little or no hypertrophy 
is noticeable, but in the older twigs slight fusiform swellings are developed. 



SAA 



III LLETIN 390 




FlG. I55. TELIOSPORES AND TELIOSPORE GERMINATION OF GYMNO- 
SPORANGIUM CLAVIPES 

The spore stalk disappears at the time of germination of the lower cell. X 350 




PlG. [56. A TELIAL SORTS OF GYMNOSPORANGIUM CLAVIPES 

The sorus is just breaking through the cork f issue. X 220 



Three Cedar Rust Kungi 



.SIS 



The I dial sori are decidedly different from the telial horns of G. Juniperi- 
virginianae and G. globosum. Instead of being long and of small diameter 
they are usually short and dome-shaped. These sori may be of various 
widths and they often coalesce and form a ring entirely around the twig. 
They are orange-brown when dry but become lighter-colored when 
gelatinized. In the latter condition they have a very soft, jelly-like 
consistency. After one or two gelatinizations the jelly-like substance 
spreads over the branches and the leaves, but later it becomes dry and 
drops off. The telial sori never recover their original shape. In on 4 
there was a period of heavy precipitation from June 20 to June 22 and 
the sori did not regain their normal form after that time. In 19 14 there 
were four gelatinization periods as compared with eleven in 19 15. During 
several of these periods of gelatinization few or no basidiospores were 
formed. Numerous cankers caused by this pathogene have been under 
observation since the spring of 19 1,3, and each year telial sori have 




FlG. 157. DIAGRAMMATIC SECTION OF CEDAR rWIG 
AFFECTED WITH GYMNOSPORANGIUM CLAVIPES 

The relative size and position of the telial sori are shown 

developed in the cankered areas. Undoubtedly the cankers were formed 
several years previous to 19 13. 

Teliospore germination. — The teliospores of this species are capable of 
germinating at about the same time in the spring and under the same 
conditions as those of G. globosum and G. Juniperi-virginianae. The 
curve in figui'e 142 (page 523), and the discussion of methods and results 
on page 522, apply to this species also. 

The spores of G. clavipes differ slightly from those of the other two 
species. They vary in length from 29 to 50 /j. and in width from 1 7 to 2 5 ^. 
They may be slightly constricted at the septum, rounded or acute at 
the apex, and obtuse at the base. The wall is yellow and is from 1 to 
2 fx thick, being slightly thickened at the apex. The pedicels may 
vary in diameter just below the spore from 7 to 50 n, depending on the 
degree of swelling. Each cell has but one pore, the pore in the upper 
cell being in the apex and that in the lower cell being on one side near 
the base of the spore. 



546 Bulletin 390 

Spores of 67. clavipes are peculiar in that often the germinating spores 
no longer have their spore stalks attached. It has been found that these 
stalks may be present if only the apical cell germinates, while, on the other 
hand, if both cells germinate the pedicels are never present or at least 
have not been seen. As soon as the basal cell begins to germinate, the side 
of the spore stalk nearest to the germ pore enlarges rapidly. The swelling 
continues until the wall of the stalk just below the germ pore finally 
disappears. Often before this stage has been reached the opposite side 
of the pedicel wall begins to disappear, so that soon only small remnants 
of the wall remain clinging to the spore. On certain slides on which 
spores were placed to germinate, absolute alcohol was added when the 
process of germination was only partially complete. The alcohol extracted 
the water, and the stalk returned to its normal shape and size. After 
the wall of the pedicel had become invisible it failed to return to view 
on the addition of alcohol. Apparently the lower promycelium develops 
at the base of the spore and thus displaces the pedicel. It is probable 
that the disappearance of the spore stalks when germination occurs accounts 
for the complete destruction of the telial sori as mentioned above. 
Numerous observations have been made to determine whether or not 
a similar phenomenon occurs in 67. globosum and 67. J uniperi-virginiauae, 
but this has never been found to be the case. In these species the pro- 
mycelium develops near the septum, so that it is not obstructed by the 
pedicel. 

The disintegration of the pedicel in G. clavipes has been noticed also 
by certain other writers. Farlow (1880) states that when quickly swollen, 
especially by the absorption of reagents, the inner part of the pedicel 
expands more quickly than the outer part, so that the latter is ruptured 
just below the spore, leaving a hyaline ring surrounding the pedicel at 
the base of the spore. Farlow's explanation of this phenomenon seems 
logical so far as it goes, but it is not clear why this process takes place 
only when it accompanies the germination of the lower cell. 

The methods of ejection and germination of the basidiospores of 
G. clavipes are identical with those described for G. Juniperi-virginianae. 

Throughout a period of three years numerous attempts were made to 
produce infection with spores of 67. clavipes on red cedar trees, but only 
negative results were obtained. 

Aecial stage 

The conditions influencing infection and the development of pyenia 
and aecia of 67. clavipes are similar to those for the other two species. 
Both fruiting structures resemble closely those of 67. Juniperi-virginianae. 
The pyenia, however, are about one-fourth larger. The peridium and 



Three Cedar Rust Pungi 547 

the peridial cells, together with the size of the aeciospores, serve as the 

distinguishing features. The aecia are much broader than those of G. 

globosum and the aeciospores measure from 21 to 32 /j. by from 24 to 39 n. 

The peridium of G. clavipes is white, while those of the other two species 

are slightly yellowish. The peridium splits longitudinally, in some cases 

to the base of the cup, but the strands may be several layers of cells in 

width. These strands may either stand erect or become more or less 

recurved at their extremities. Kern (1911:455) describes the peridial 

cells as follows: 

Peridial cells seen in both Eace and side views, pulygoiial-ovate or polygonal oblong 
in faee view, 19-39 x 45-95 m, rhomboid in side view, 25-40 m thick, outer wall moderately 
thick, 3-5 m, inner wall very thick, 13-23 u, coarsely verrucose with loosely set, large, 
irregularly branched papillae, side walls verrucose on inner half similar to inner wall. 



S |.", Ill l.l.l'.TIN 390 



LITERATURE CITED 

Blackman, Vernon H. On the conditions of teleutospore germination 
and of sporidia formation in the Uredineas. New phytol. 2:10-14. 
1903. 

Buller, A. II. Reginald. The violent projection of spores from the 
hymenium — Methods 1, 11, in, iv, and v. In Researches on fungi, 

Chester, Frederick D. Apple rust. /// Report of the Mycologist. 

Delaware Coll. Agr. Exp. Sta. Rept. 8:63-69. 1896. 
Coons, George Herbert. Some investigations of the cedar rust fungus, 

Gymnosporangium juniperi-virginianae. Nebraska Agr. Exp. Sta. 

Rept. 25:215-245. 191 2. 
Crabill, C. H. Production of secondary sporidia by Gymnosporangium. 

Phytopath. 3: 282-284. I 9 I 3- 
Emerson, R. A. Apple scab and cedar rust. Nebraska Agr. Exp. Sta. 

Bui. 88: 1-2 1. 1905. 
Farlow, W. G. The Gymnosporangia or cedar-apples of the United 

States. Boston Soc. Nat. Hist. Anniversary memoirs, p. 1-38. 1880. 
The development of the Gymnosporangia of the United Stales. 

Bot. gaz. 11:234-241. 1886. 
Giddings, N. J., and Berg, Anthony. Apple rust. West Virginia 

Univ. Agr. Exp. Sta. Bui. [54:1-73. 1915. 
Giddings, N. J., and Neal, D. C. Control of apple rust by spraying. 

Phytopath. 2:258-260. 191 2. 
Heald, F. D. The life history of the cedar rust fungus Gymnosporangium 

juniperi-virginianae Schw. Nebraska Agr. Exp. Sta. Rept. 22:105 

113. 1909. 
Kern, Frank D. Studies in the genus Gymnosporangium. Torrey Bot. 

Club. Bui. 35:499-511. 1908. 
A biologic and taxonomic study of the genus Gymnosporangium. 

New York Bot. Gard. Bui. 7:391-483. 191 1. 
Link, H. F. Gymnosporangium macropus. Willdenow, Species plan- 

tarum (Linne) 6 2 :i28. 1825. 
Pammel, L. H. The cedar apple fungi and apple rust in Iowa. Iowa 

Agr. Exp. Sta. Bui. 84:1-36. 1905. 
Peck, Chas. H. Report of the Botanist. New York State Mus. Nat. 

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Report of the Botanist. New York State Mus. Nat. Hist. 

Rept. 26:35-91. 1874. 
Reed, Howard S., Cooley, J. S., and Crabill, C. H. Experiments on 

the control of the cedar rust of apples. Virginia Polytech. Inst. Agr. 

Exp. Sta. Bui. 203:1-28. 1914. 
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caused by Gymnosporangium Juniperi-Virginianae Schw. Virginia 

Polytech. Inst. Agr. Exp. Sta. Tech. bul. 9:1-106. 1915. 
Sanford, Elmer. Microscopical anatomy of the common cedar-apple 

(Gymnosporangium macropus) . Ann. bot. 1:263-268. 1888. 



Three Cedar Rust Fungi 549 

Schweinitz, Ludovici Davidis de. Gymnosporangium Decand. hi 

Synopsis fungorum Carolinae superioris. Schrift. Naturf. Gesell. 

1:74-75. 1822. 

Subgen. Roestelia aut ceratites. In Synopsis fungorum in 

America boreali media degentium. Amer. Phil. Soc. Trans, n. s. 

4:294. 1834. 
Smith, R. I., and Stevens, F. L. Insects and fungous diseases of apple 

and pear. North Carolina Agr. Exp. Sta. Bui. 206:43-126. 1910. 
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(Geneva) Agr. Exp. Sta. Bui. 328:305-404. 1910. 
Stewart, F. C, and Carver, G. W. Inoculation experiments with 

Gymnosporangium macropus, Lk. New York (Geneva) Agr. Exp. Sta. 

Rept. 14:535-544. 1896. 
Stone, G. E. An outbreak of rusts. Massachusetts Agr. Exp. Sta. 

Rept. 23 : 144. 191 1. 
Stone, R. E. Cedar apples and apple leaf -rust. Alabama Agr. Exp. 

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ran^inm-Arten hervorgerufenen Missbildungen. Forst. Nat. Zeitsch". 

3 : 68 84, 129-172. 1894. 



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